Sci Nat (2017) 104: 26 DOI 10.1007/s00114-017-1455-7

SHORT COMMUNICATION

The first direct evidence of a Late Devonian coelacanth fish feeding on conodont animals

Michał Zatoń1 & Krzysztof Broda1 & Martin Qvarnström2 & Grzegorz Niedźwiedzki2 & Per Erik Ahlberg2

Received: 9 February 2017 /Revised: 28 February 2017 /Accepted: 2 March 2017 /Published online: 10 March 2017 # The Author(s) 2017. This article is published with open access at Springerlink.com

Abstract We describe the first known occurrence of a Introduction Devonian coelacanth specimen from the lower Famennian of the Holy Cross Mountains, Poland, with a conodont Coelacanths are sarcopterygian fishes which have a long evo- element preserved in its digestive tract. A small spiral lutionary history ranging back to the Early Devonian (Zhu and phosphatic coprolite (fossil excrement) containing et al. 2012). The group comprised numerous species in numerous conodont elements and other unrecognized re- the geological past, but today is represented by the single mains was also found in the same deposits. The coprolite genus Latimeria, first discovered in 1938 in the Indian is tentatively attributed to the coelacanth. Although it is Ocean. Although the extant Latimeria occupies a deep-sea unclear whether the Late Devonian coelacanth from habitat, fossil coelacanths inhabited a range of different Poland was an active predator or a scavenger, these finds palaeoenvironments and evidently occupied various ecologi- provide the first direct evidence of feeding on conodont cal niches, as indicated by their occurrence in different facies animals by early coelacanth fish, and one of the few and their morphological disparity (Friedman and Coates 2006; evidences of feeding on these animals known to date. It Wendruff and Wilson 2012). Despite growing knowledge also expands our knowledge about the diet and trophic about fossil coelacanth diversity, disparity, anatomy, and even relations between the Paleozoic marine animals in ontogeny (Wendruff and Wilson 2012; Gess and Coates general. 2015), there is still insufficient data on some important palaeobiological aspects, including diets. Gut contents are an important source of direct evidence on food gathering by fos- Keywords Coelacanth . Conodonts . Gut content . sil organisms, including fishes. These, however, are extremely Coprolite . Devonian rare in fossil coelacanths. To date, recognizable gut contents have been recorded in only two species. Lund and Lund (1984, 1985) found scales and even an intact paleostomatopod shrimp in the species Caridosuctor Communicated by: Sven Thatje populosum from the Lower Carboniferous Bear Gulch Limestone of MT, USA. Clement (2005)foundaganoidscale, Electronic supplementary material The online version of this article (doi:10.1007/s00114-017-1455-7) contains supplementary material, arthropod appendages, and a crushed, incomplete crustacean which is available to authorized users. within the body cavity of Wenzia latimerae from the Upper Jurassic of France. Recently, Yabumoto and Brito (2013)re- * Michał Zatoń ported some unrecognizable stomach contents in the [email protected] mawsoniid coelacanth Axelrodichthys araripensis from the Lower Cretaceous Crato Formation of Brazil. 1 Faculty of Earth Sciences, University of Silesia, Będzińska 60, In the present paper, we report the presence of a single 41-200 Sosnowiec, Poland conodont element from the gut content of a coelacanth spec- 2 – Department of Organismal Biology, Uppsala University, imen (Fig. 1a b) from the Upper Devonian deposits of Norbyvägen 18A, 752 36 Uppsala, Sweden Poland. Additionally, several conodont elements have also 26 Page 2 of 5 Sci Nat (2017) 104: 26

Fig. 1 a Coelacanth fish, specimen GIUS 4–3654/1. b Conodont organization of this specimen. h head, op opercula, tf tail fin. Scale bars element found in its digestive tract. c Conodont-bearing, spiral coprolite 10 mm (a), 0.2 mm (b), and 3 mm (c–d) specimen GIUS 4–3624/4. d Virtual thin section showing spiral internal

been detected within a phosphatic and spiral coprolite found in Results the same deposits (Fig. 1c–d). The gut content, and possibly the coprolite, is the first direct evidence for feeding on cono- The coelacanth found in the lower Famennian deposits is not dont animals by Late Devonian coelacanth fishes. well-preserved, but represents an articulated skeleton consisting of part and counterpart. The general characteristics of the skeleton, especially the morphology of the gular plates and opercula, suggest that the coelacanth may represent, or be Material and methods closely related to, the genus Diplocercides, of which isolated remains are known from other Famennian localities in the The coelacanth fish and conodont-bearing coprolite were Holy Cross Mountains (Szrek 2007). However, a more precise found in the Upper Devonian (lower Famennian) marly identification is difficult due to the poor preservation of the shales outcropping in the Kowala quarry, Holy Cross cranial skeleton. The length of the specimen is 15 cm from the Mountains, Poland. These deposits are already known to tip of its snout to the posterior end of its caudal fin. The yield abundant phosphatized arthropod cuticles and copro- conodont element has been found embedded within a light- lites (Zatoń et al. 2014;Zatoń and Rakociński 2014). Both brown phosphatic mass occurring in the posterior part of the the coelacanth fossil and the spiral coprolite were exam- coelacanth (Fig. 1a). The conodont is represented by a plat- ined uncoated and under low vacuum condition using a form element most likely representing the polygnathid genus Philips XL30 environmental scanning electron microscope Ctenopolygnathus. It is 1.5 mm long and its surface is well- (ESEM). Both the stomach content and the coprolite fossil preserved, lacking any signs of etching caused by digestive inclusions (that were visible on the exterior) were docu- processes (Fig. 1b). mented using back-scattered electron (BSE) imaging. Synchrotron microtomography showed that the spiral cop- Additionally, in order to retrieve high-resolution, three- rolite (Fig. 1c–d)containsnumerousconodontinclusions,in- dimensional data from both the coprolite’sexteriorand cluding four pectiniform elements and many isolated interior, it was scanned using propagation phase-contrast coniform elements (Fig. 2b, e). The recognizable Pa-element synchrotron microtomography (PPC-SRμCT) at beamline is similar to the species Mehlina kielcensis (Fig. 2f). The co- ID19 of the European Synchrotron Radiation Facility nodont inclusions occur in a dense coprolite matrix (Fig. 2a, (ESRF), France (Supplementary info). c–d) which in part probably represent other digested parts of The specimens are housed at the Faculty of Earth the conodont jaw apparatus or digested biomineralized struc- Sciences, University of Silesia, Sosnowiec, Poland, ab- tures. Additionally, elongated, less dense structures with breviated GIUS 4-3654/1 (coelacanth) and GIUS 4- etched extremities occur in association with the conodont 3624/4 (coprolite). teeth (Fig. 2d). It is possible that these elements also originate Sci Nat (2017) 104: 26 Page 3 of 5 26

Fig. 2 Conodont tooth elements found in the scanned coprolite. a Virtual pectiniform element (white arrow), and elongated enigmatic structures of thin section showing one pectiniform and several coniform conodont possible conodont origin (long arrows). e Segmented conodont tooth tooth elements (white arrows). b Segmented conodont tooth elements, elements and dense coprolite matrix, probably representing digested where the lowest specimen is the same pectiniform element as shown in a. biomineralized tissues. f Polygnathid conodont element similar to c Virtual thin section showing biomineralized structures and conodont Mehlina kielcensis. co coprolite mass, hs host sediment, a air. Scale tooth element (white arrow). d A virtual thin section of the coprolite bars 0.6 mm (a), 0.2 mm (bi), 0.15 mm (bii, biii), 0.5 mm (c), 0.85 mm showing dense accumulation of digested biomineralized structures, one (d), 0.25 mm (e), and 0.05 mm (f) from the jaw apparatus or other parts of the conodont animal, (Oulodus and Icriodus), have been found within the gut region but poor preservation rules out more precise identification. of a palaeoniscoid fish from the Upper Devonian Gogo Another coprolite (9.5 mm long and 8.3 mm wide) found in Formation in Australia by Nicoll (1977). In the same formation, the same lower Famennian deposits at the Kowala quarry has Choo et al. (2009) found a basal actinopterygian fish previously been shown using ESEM to contain a single cono- Gogosardina with prioniodinid conodont elements preserved dont element embedded within a phosphatic fecal mass (Zatoń in its branchial regions. Williams (1990) noted conodont ele- and Rakociński 2014). ments inside 9% of all specimens of Cladoselache sharks from the Famennian Cleveland Shale of Ohio. Conodont elements have also been found within the enigmatic metazoan called Discussion Typhloesus wellsi from the Carboniferous Bear Gulch Limestone in Montana (Conway Morris 1990). The presence of a conodont element within the Famennian Thus, the find not only supports the earlier notions that coelacanth is not the result of any post-mortem process, as it conodont animals, the extinct chordates (Purnell et al. 1995) is clearly embedded within the phosphatic mass occurring be- which were particularly abundant in the Late Devonian seas tween the part and counterpart of the preserved fish. Therefore, (Dzik 2002), were ideal prey for various Devonian fishes, but its occurrence must reflect feeding on the conodont animal by also expands our knowledge about the diet of the Late the coelacanth. This is the first direct evidence of feeding on Devonian coelacanths. However, the presence of only a single conodont animals by early coelacanth fishes, and also one of conodont element within the body cavity of a coelacanth does the few evidences of feeding on these animals in general. not provide any clue as to whether the fish actively hunted Previously, conodonts, belonging to two multielement taxa living conodont animals or scavenged carcasses lying on the 26 Page 4 of 5 Sci Nat (2017) 104: 26 seafloor. It is known that the living species Latimeria Acknowledgments This work was supported by the NCN grant chalumnae is a predominantly piscivorous benthic or 2015/19/N/ST10/01527 (for K.B.). G.N. is currently funded by a Wallenberg Scholarship grant awarded to P.E. Ahlberg (Uppsala epibenthic feeder (Uyeno and Tsutsumi 1991). The stomach University). M.Q. is funded by a grant from the Swedish Research contents preserved in some fossil coelacanths, mainly Council awarded to ŽivilėŽigaitė (Uppsala University). The scans were consisting of arthropods (Lund and Lund 1984, 1985; performed at the ESRF (Grenoble, France) as a part of the project ES145. Clement 2005), are also suggestive of feeding principally on Many thanks to Paul Tafforeau at the ESRF for extensive help with imaging and reconstructions of the scanned data. benthic animals. Thus, we cannot exclude that the Late Devonian coelacanth from Kowala was a benthic scavenger. Open Access This article is distributed under the terms of the Creative However, we must also bear in mind that early coelacanth Commons Attribution 4.0 International License (http:// creativecommons.org/licenses/by/4.0/), which permits unrestricted use, species were morphologically very diverse (Friedman and distribution, and reproduction in any medium, provided you give Coates 2006; Wendruff and Wilson 2012) and thus their niche appropriate credit to the original author(s) and the source, provide a link partitioning, along with feeding preferences, certainly varied to the Creative Commons license, and indicate if changes were made. as well. Interestingly, the same lower Famennian, coelacanth-bearing deposits contain numerous fish coprolites. Recently, a coprolite References containing a single conodont element has been found in the Kowala quarry by Zatoń and Rakociński (2014). Earlier, Dzik Choo B, Long JA, Trinajstic K (2009) A new genus and species of basal (2002) illustrated conodont elements aggregated together (prob- actinopterygian fish from the Upper Devonian Gogo Formation of – ably representing coprolite contents) from the basal Famennian Western Australia. Acta Zool-Stokholm 90(Suppl. 1):194 210 ł Clement G (2005) A new coelacanth (Actinistia, Sarcopterygii) from the of P ucki, Holy Cross Mountains. Conodonts enclosed within Jurassic of France, and the question of the closest relative fossil to phosphatic coprolites have also been noted in the lower Latimeria. J. Vert. Paleontol. 25:481–491 Famennian Cleveland Shale in OH, USA by Williams (1990). Conway Morris S (1990) Typhloesus wellsi (Melton and Scott, 1973), a The new coprolite reported here contains several platform bizarre metazoan from the Carboniferous of Montana, USA. Philos T Roy Soc B 327:595–624 and conical conodont elements. Of course, identification of a Dzik J (2002) Emergence and collapse of the Frasnian conodont and producer based on the coprolite itself is always speculative. ammonoid communities in the Holy Cross Mountains, Poland. However, it is possible that at least some of the coprolites Acta Palaeontol Pol 47:565–650 reported earlier by Zatoń and Rakociński (2014) and that pre- Friedman M, Coates MI (2006) A newly recognized coelacanth high- sented here may have been produced by coelacanth fish, the lights the early morphological diversification of the clade. P Roy Soc B 273:245–250 disarticulated remains of which are common in the deposits Gess RW, Coates MI (2015) Fossil juvenile coelacanths from the investigated (Zatoń and Broda 2015). Apart from the Devonian of South Africa shed light on the order of character ac- supporting evidence in the form of a conodont element pre- quisition in actinistians. Zool J Linnean Soc 175:360–383 – served within a coelacanth fish shown here, the spiral internal Ginter M (2002) Chondrichthyan fauna of the Frasnian Famennian boundary beds in Poland. Acta Palaeontol Pol 47:329–338 organization of the coprolite may be relevant (Fig. 1d). It is Lund R, Lund WL (1984) New genera of coelacanths from the Bear known that coelacanth fishes possess a spiral gut valve Gulch Limestone (Lower Carboniferous) of Montana (USA). (Thoney and Hargis 1991). Moreover, the very small sizes Geobios 17:237–244 of the lower Famennian coprolites from Kowala, which range Lund R, Lund WL (1985) Coelacanths from the Bear Gulch Limestone only from 6 to 18 mm in length (Zatoń and Rakociński 2014), (Namurian) of Montana and the evolution of the Coelacanthiformes. Bull Carnegie Mus Nat Hist 25:1–74 are comparable to the size of the coelacanth discussed. Nicoll RS (1977) Conodont apparatuses in an Upper Devonian The relative diversity of fishes from the lower Famennian palaeoniscoid fish from the Canning Basin, Western Australia. (crepida conodont Zone) deposits may indicate coelacanths as BMR J Aus Geol Geophys 2:217–228 producers of at least some of the coprolites. Other fish remains Purnell MA, Aldridge RJ, Donoghue PCJ, Gabbott SE (1995) Conodonts and the first vertebrates. Endeavour 19:20–27 are known in these deposits. Sharks and acanthodians are Szrek P (2007) Coelacanths (Actinistia, Sarcopterygii) from the known from their teeth and scales (Ginter 2002) and ganoid Famennian (Upper Devonian) of the Holy Cross Mountains, fishes as scales inside coprolites (Zatoń and Rakociński 2014). Poland. Acta Geol Pol 57:403–413 However, the coelacanth remains are the most numerous fos- Thoney DA, Hargis WJ Jr (1991) Juvenile anisakine parasites from the – sils occurring in these deposits. To date, incomplete coela- coelacanth Latimeria chalumnae. Environ Biol Fish 32:281 283 Uyeno T, Tsutsumi T (1991) Stomach contents of Latimeria chalumnae canth remains comprise 23 specimens represented either by and further notes on its feeding habits. Environ Biol Fish 32:275–279 isolated opercula or associated cranial elements (Zatoń and Wendruff AJ, Wilson MVH (2012) A fork-tailed coelacanth, Rebellatrix Broda 2015). Other coelacanth remains (Diplocercides sp.) divaricerca, gen. et sp. nov.(Actinistia, Rebellatricidae, fam. nov.), have also been reported from deposits of the same conodont from the Lower Triassic of Western Canada. J Vert Paleontol 32: 499–511 zone in the Wietrznia locality (Szrek 2007). Thus, it seems Williams ME (1990) Feeding behavior in Cleveland shale fishes. In: that the lower Famennian crepida conodont Zone deposits Boucot AJ (ed) Evolutionary paleobiology of behavior and coevo- are particularly rich in coelacanths. lution. Elsevier, Amsterdam, pp 273–287 Sci Nat (2017) 104: 26 Page 5 of 5 26

Yabumoto Y, Brito PM (2013) The second record of a mawsoniid coela- Zatoń M, Rakociński M (2014) Coprolite evidence for carnivorous pre- canth from the Lower Cretaceous Crato Formation, Araripe Basin, dation in a Late Devonian pelagic environment of southern northeasthern Brazil, with comments on the development of coela- Laurussia. Palaeogeogr Palaeoclimatol Palaeoecol 394:1–11 canths. In: Arratia G, Schultze H-P, Wilson MVH (eds) Mesozoic Zatoń M, Filipiak P, Rakociński M, Krawczyński W (2014) Kowala fishes 5. Global diversity and evolution. Verlag Dr. F. Pfeil, Munich, Lagerstätte: Late Devonian arthropods and non-biomineralized al- pp 489–497 gae from Poland. Lethaia 47:352–364 Zatoń M, Broda K (2015) First record of soft tissue preservation in the Zhu M, Yu X, Lu J, Qiao T, Zhao W, Jia L (2012) Earliest known coela- Upper Devonian of Poland. PLoS One 10:e0142619. doi:10.1371/ canth skull extends the range of anatomically modern coelacanths to journal.pone.0142619 the Early Devonian. Nat Commun 3:772. doi:10.1038/ncomms1764